Barbara K. Giza

Issues of gustatory neural coding: where they stand today.

The basic issues of gustatory neural coding are revisited. Questions addressed and conclusions drawn are: (1) what is the physical dimension across which gustatory neurons are sensitive, and upon which taste perceptions are based? The dimension that unites the various taste qualities is not physical, but physiological: a dimension of well-being, bounded by toxins at one extreme and nutrients at the other. (2) How broadly tuned are taste cells across the dimension? There are instances of specificity, but most mammalian taste cells respond to a range of qualities. (3) Are there basic taste qualities? Sweet, salty, sour, and bitter are widely accepted as basic tastes. Umami and starch tastes are considered basic by some. (4) Is taste topographically organized? There is some degree of physical separation among neurons most responsive to different taste qualities, but this does not appear to be sufficient precision to act as a meaningful coding mechanism. (5) Are there gustatory neuron types? Neurons, separated into categories according to their response profiles, respond as members of their category to the challenges of conditioned aversions and preferences, sodium deprivation, hyperglycemia, and receptor blockade, while cells from other categories react differently. This indicates the existence of functionally distinct types of taste cells. (6) Is the quality signal coded within the activity of the single most appropriate category of neurons, or is it carried by the pattern of response across neuronal categories? Both the breadth of responsiveness and the logical ambiguity of the signal in any one category of neurons argue that the taste message is carried by a pattern of activity across gustatory neuron types.

Polysaccharides as taste stimuli: their effect in the nucleus tractus solitarius of the rat

Rats show a pronounced preference for the tastes of starch-derived polysaccharides. Three of these compounds--Polycose, maltotriose and amylopectin--were used along with a standard array of chemicals in a study of their effectiveness as taste stimuli, as monitored by evoked single unit activity in the nucleus tractus solitarii (NTS). Maltotriose and amylopectin elicited very few spikes and no clear quality-related pattern of neural activity. Polycose, however, was an effective taste stimulus. It evoked an activity profile across neurons and over time that was poorly correlated with that of the prototypical sugar (sucrose) and only moderately related to those of the non-sugar prototypes (NaCl, HCl and quinine-HCl). The 14 cells (23%) that responded particularly well to Polycose were all members of neuronal subgroups that emphasized salt, acid and quinine sensitivity. Thus, despite the strong behavioral preference shown to Polycose, its neural profile is unlike those of other preferred stimuli. Polycose may represent a unique taste stimulus whose quality cannot be readily associated with those of the traditional 4 basic tastes.

Administration of satiety factors and gustatory responsiveness in the nucleus tractus solitarius of the rat

The administration of certain factors associated with postprandial satiety decreases gustatory responsiveness. We compared the effects of intravenous injections of glucose, insulin, pancreatic glucagon (PG), and cholecystokinin (CCK) on multiunit activity evoked from taste responsive neurons in the nucleus tractus solitarius of rats. Glucose, insulin, and PG reliably suppressed evoked responses to lingual application of 1.0M glucose, whereas responses that followed CCK remained unchanged. A common physiological consequence of glucose, insulin, and glucagon is increased glucose availability which may impact directly on gustatory neurons or indirectly through modifications in ventral forebrain or vagal afferent activity.

Extinction of a Conditioned Taste Aversion in Rats: II. Neural Effects in the Nucleus of the Solitary Tract

The formation of a conditioned taste aversion (CTA) in rats results in neural changes at several levels of the gustatory system. In the nucleus of the solitary tract (NTS), the outstanding feature of the response to a CS is a brief burst of activity that is absent in unconditioned animals. The burst occurs about 1 s after stimulus onset and is seen only in neurons that respond well to sugars and the CS (0.0025 M NaSaccharin). We recorded single neuron activity in response to 12 stimuli from taste cells in the NTS of 8 rats, in which a CTA to NaSaccharin had been created and fully extinguished, and in 8 unconditioned controls. The issue was if the neural effects of the CTA in NTS were reversed with extinction. We recorded the activity of 41 neurons in controls and 55 in CTA-extinguished rats. Responses measured across all neurons were not significantly different in spontaneous activity, breadth of tuning, overall response magnitude to each of the 12 stimuli, relationship among stimuli in taste spaces, or time-course. However, cells in the sugar-sensitive subgroup showed a clear vestige of the conditioning experience. They gave a well-defined burst of activity to the CS, though of reduced amplitude and slightly longer latency than in fully conditioned rats. This burst was no longer associated with the conditioned behavior-which was fully extinguished-though it may be a permanent marker for the once-salient CS that can influence subsequent reacquisition of the aversion.

A measure of taste intensity discrimination in the rat through conditioned taste aversions

The ability of rats to make intensity discriminations was determined by forming a conditioned taste aversion to a moderate concentration of each of four basic taste stimuli, and then measuring the level of acceptance (number of licks during a 15 sec exposure) shown to a range of concentrations of the same chemical. Rats (N = 66) could discriminate between glucose concentrations that were separated by as little as 0.074 M, between NaCl concentrations that differed by 0.029 M, between HCl concentrations that were 9 X 10(-4) M apart, and between quinine HCl concentrations that differed by as little as 2.4 X 10(-6) M.

Extinction of a conditioned taste aversion in rats: I. Behavioral effects.

The literature is divided over whether a conditioned taste aversion (CTA) can be fully extinguished. In Experiment 1, we created a powerful aversion in 54 rats by pairing the taste of 0.0025 M NaSaccharin (CS) with intraperitoneal injections of 127 mg/kg LiCl (US) on 3 occasions. We then offered 23-h deprived rats NaSaccharin for 10 min/day to observe the course of recovery. Extinction occurred in three phases: static, dynamic, and asymptotic. During the static phase (mean = 9.6 days), rats consumed the CS at < 10% of their preconditioned rate. With dynamic recovery (6.0 days), they increased acceptance to > 80% of preconditioning levels. Finally, they achieved asymptote (3.1 days) at 100% acceptance. In Experiment 2, we used 8 additional conditioned rats and 8 unconditioned controls. We followed the same 1-bottle extinction procedure and, again, obtained 100% acceptance. Then we offered both NaSaccharin and water for 8 days at 23 h/day and monitored lick patterns every 6 s to determine taste preferences. The conditioned animals consumed less NaSaccharin than controls on Day 1, and less NaSaccharin as a percentage of total fluid as late as Day 3. For the last 5 days of 2-bottle preference testing, there were no significant differences between the groups with regard to 1. volume of NaSaccharin or water consumed, 2. percentage of total fluid taken as NaSaccharin, 3. consumption of each fluid associated with a meal or taken spontaneously, 4. intake during the light or dark periods, or 5. the characteristics of ingestion, including number of drinking bouts, duration of bouts, number of licks/bout, and rate of licking. Therefore, a robust CTA is subject to complete behavioral extinction.

Blood glucose level affects perceived sweetness intensity in rats

Electrophysiological data indicate that hyperglycemia is associated with decreased neural taste responsiveness to 1.0 M glucose, but not to 0.01 M quinine HCl, in the rats hindbrain. The present behavioral experiment was conducted to determine whether this suppression of neural activity is manifested in a reduced intensity perception to glucose, but not quinine. Each rat learned to avoid 1.0 M glucose through development of a conditioned taste aversion. Perceived intensity was then measured in control and in hyperglycemic rats by the extent to which they generalized to each test concentration of glucose. Experimental subjects treated moderate glucose concentrations (0.6-2.0 M) as if their intensity perceptions were reduced by 47%. This is consistent with the mean reduction of 43% in taste-evoked neural activity associated with hyperglycemia. A corresponding experiment gave no indication of a change in intensity perception to quinine as a function of hyperglycemia, again in accord with earlier electrophysiological results. We conclude that nutritional state may selectively affect gustatory sensitivity in the rat.

Preference conditioning alters taste responses in the nucleus of the solitary tract of the rat

Aversive conditioning has an impact on the neural signal for the gustatory conditioned stimulus (CS). Here, we determined whether the code is also affected by preference conditioning. We paired the taste of MgCl2 (CS+) with intragastric nutrients in some rats (MG), and citric acid (CS+) with nutrients in others (CI). A control group (Control) experienced both tastants without nutrients. Preferences (>90%) developed for each CS+. We recorded responses to 16 taste stimuli in the nucleus of the solitary tract. Responsiveness of acid-oriented neurons to MgCl2 in MG rats was lower than in Controls, and its profile was more distinct from those of acidic and bitter stimuli. Total activity to citric acid was unchanged in CI rats. However, its temporal profile showed a decreased phasic component, making citric acid temporally distinct from nonsugars. Therefore, the responses to both CS+ were modified, each in its own manner, to be more distinct from those of aversive stimuli. The effects of preference conditioning, however, were weaker than those of aversive conditioning.Aversive conditioning has an impact on the neural signal for the gustatory conditioned stimulus (CS). Here, we determined whether the code is also affected by preference conditioning. We paired the taste of MgCl2 (CS+) with intragastric nutrients in some rats (MG), and citric acid (CS+) with nutrients in others (CI). A control group (Control) experienced both tastants without nutrients. Preferences (>90%) developed for each CS+. We recorded responses to 16 taste stimuli in the nucleus of the solitary tract. Responsiveness of acid-oriented neurons to MgCl2 in MG rats was lower than in Controls, and its profile was more distinct from those of acidic and bitter stimuli. Total activity to citric acid was unchanged in CI rats. However, its temporal profile showed a decreased phasic component, making citric acid temporally distinct from nonsugars. Therefore, the responses to both CS+ were modified, each in its own manner, to be more distinct from those of aversive stimuli. The effects of preference conditioning, however, were weaker than those of aversive conditioning.

Activity in rat nucleus tractus solitarius after recovery from sodium deprivation.

Sodium depletion has powerful effects on ingestive behavior. Depleted rats consume NaCl avidly at first, but decrease their intake to normal levels as they restore their sodium balance. However, vestiges of the depletion experience are expressed as a more rapidly induced and robust sodium consumption when the rat is challenged with a second depletion. Thus, the salience of sodium to the rat is modified in a lasting manner by severe deprivation. Sodium depletion also causes changes in the responses of taste cells in the nucleus tractus solitarius (NTS). In the present study, we examined whether gustatory-evoked responses in rat NTS continue to reflect the condition induced by sodium deprivation after sodium balance is restored. Single-unit recordings were made in response to 13 taste stimuli in two groups of rats: an experimental group that underwent 10-16 days of sodium deprivation followed by a 2-week recovery period, and a control group that never experienced deprivation. Experimental animals were tested for daily intake of 0.5 M NaCl before and after deprivation; they demonstrated a clear salt appetite only on the first day of the recovery period. Electrophysiological recordings revealed no significant differences between the two groups in response to any single stimulus. Neurons from each group of rats were categorized into three subtypes: sugar-sensitive, salt-sensitive, and nonsugar cells. A comparison of responses in these three subtypes offered no significant differences across groups. Thus, as rats restore depleted sodium levels following deprivation, the responsiveness of cells in the NTS also returns to a predeprivation state.

Neurophysiological Aspects of Sweetness

In the natural environment, sweetness can nearly always be equated with energy. Consequently its detection is associated with a powerful hedonic appeal which declines only as energy needs are met. In this chapter we will first describe the sensory code by which sweet stimuli are represented and then discuss the neural basis of the hedonic response to sweetness and its malleability by physiological need.